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Symbiosis Between Methane-Oxidizing Bacteria and a Deep-Sea Carnivorous Cladorhizid Sponge

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Symbiosis Between Methane-Oxidizing Bacteria and a Deep-Sea Carnivorous Cladorhizid Sponge MARINE ECOLOGY PROGRESS SERIES Published December 31 Mar Ecol Proy Ser Symbiosis between methane-oxidizing bacteria and a deep-sea carnivorous cladorhizid sponge Jean ~acelet'v*,Aline ~iala-~edioni~,C. R. is her^, Nicole Boury-Esnaultl 'Centre d'oceanologie de Marseille, Universite de la Mediterranee - UMR CNRS no. 6540, Station Marine d'Endoume, F-13007 Marseille, France 20bservatoireOceanoloyique. Laboratoire Arayo, F-66650 Banyuls-sur-Mer, France 3Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802. USA ABSTRACT Dense bush-l~keclumps of several hundred ~nd~vldualsof a new specles of Cladorhiza (Demosponglae, Poeciloscler~da)were observed near methane sources in mud volcanoes 4718 to 4943 m dcep In the Barbddos Trench The sponge tissue contalns 2 maln mo~pholog~caltypes of extra- cellular symbiotic bacteria small rod-shaped cells and larger cocco~dcells with stacked membranes Stdble carbon ~sotopevalues, the presence of methanol dehydrogenase and ultrastructural observa- tlons all lndlcate that at least some of the syrnblonts are methdnotrophic Ultrastructural ev~denceof ~nlracell~~lard~gest~on of thp syn~b~ontsand the stable C and X values suggest that thc sponge obtalns a slgnlflcdnt portion of its nutr~tlonfrom the symbionts Ultrdstructure of the sponqe embryo suggests d~recttransmission throuqh qc.neratlons In brooded embryos The sponge also ma~ntrilnsa carnivorous feed~nghdblt on tin\ swlmmlng prey, as do other cladorhlzlds KEY L\/ORDS. Methanotrophy POI-~fera. Deep-sea . Symbiosis . Cold-seep communities INTRODUCTION although they are sometimes abundant on extinct chimneys (Boury-Esnault & De Vos 1988) or in vent Associations between several phyla of marine inver- peripheral areas. The lack of sponges in most tebrates and chemoautotrophic sulfur-oxidizing and/or chemosynthetic communities i.s rather surprising as methanotrophic bacteria are frequently found in they are probably the marine invertebrates in which marine communities surrounding hydrothermal vents, symbiosis with the widest variety of microsymbionts, cold seeps, and other reducing envi.ronments (Chil- algae and heterotrophic bacteria occurs (Vacelet & dress et al. 1986, Fiala-Medioni & Felbeck 1990, Donadey 1977, Wilkinson 1987, 1992). All sponge spe- Cavanaugh 1993, Nelson & Fisher 1995).These associ- cies examined to date are associated with microsym- ations often dominate deep-sea communities depend- bionts, and in the case of 'bacteriosponges' the sym- ing on chernosynthesis, locally resulting in a high den- bionts may constitute more than one-third of the total sity of invertebrates. These oases of life have a fauna1 tissue volume (Vacelet 1975, Reiswig 1981). However, biornass several orders of magnitude higher than that until very recently, associations with methanotrophic of the surrounding deep sea (Grassle 1986, Tunnicliffe bacteria were not described in the Porifera. 1991). The discrete participation of sponges in deep-sea Sponges had not previously been documented ecosystems directly depending on chemosynthesis among the dense assemblages of invertebrates thriv- may be due to the absence of adaptations of these ing in hydrothermal vent effl.uents (Tunnicliffe 1991), sedentary organisms to life in such harsh, rapidly changing environments (Grassle 1986). However, it is also possible that sponges are more abundant in these assemblages than previously thought, given the poor knowledge of the distribution, biology and cytology of 0 Inter-Research 1996 Resale of full at-tide not permitted Mar Ecol Proy Ser 145: 77-85, 1996 deep-sea sponges. Recently, associations between for direct transmission of the bacteria through genera- demosponges and methanotrophic bacteria occurring tions. near methane sources have been reported in the deep sea (Harrison et al. 1994, Vacelet et al. 1995) and in the deep lake Baikal, Irkutsh (Efremova et al. 1995). The MATERIALS AND METHODS association apparently results in an unusual abun- dance of sponges near the hydrocarbon sources. Sampling. Specimens (Fig 1) were collected from Here we describe one of these associations, which mud volcano fields in the Barbados Trench during the was first reported, in 1995 (Vacelet & Boury-Esnault 'Baresnaut' (1987) and 'Manon' (1992) cruises (Henry 1995) The host, a carnivorous sponge without an et al. 1990, Le Plchon et al. 1990, Olu et al. in press). aquiferous system, is abundant around deep-sea mud Field observations and collections were made by volca.noes near the Barbados accretionary prism. It means of the submersible 'Nautile' (IFREMER) on the harbors 2, possibly 3, morphological types of bacteria. diatreme Atalante during the d.i.ves Manon MAO1 The tissue 6'" and diNvalues, the presence of a key (13" 49' 36" N, 57" 39' 58" W, 4943 m) and Baresnaut enzyme of methanotrophy in the sponge tissue, the PL 94/3 (13" 49' N, 57" 38' W, 4935 m), and on the habitus and distribution of the animal, and the ultra- diapir Mount Manon during the dive Manon MA06 structure of some symbionts all support the thesis that (13" 46' 74" N. 57" 32' 51" W, 4718 m). at least some of the symbionts are methanotrophic. Immediately after recovery, small samples of the Ultrastructural evidence is presented for intracellular specimens from the Manon cruise were either pre- phagocytic digestion of the bacteria by the sponge and served for cytology or frozen. The remaining speci- Fig. 1. Cladorhiza sp. Large bush of cladorhizid sponges, approximately 40 cm high, observed from the submersible 'Nautile' at 4943 m in the mud volcano Atalante in the Barbados Trench. The bushes were most abundant and larger around the periphery of the mud-volcano eye where the largest amounts of methane were detected (OIFREMER) Vacelet et al.: Bacteria-sponge symbios~s 79 mens, approximately 100 individuals, were preserved nized around a dense central axis of spicules. It con- in alcohol. The sponge is a new species of Cladorhiza tained ovoid embryos 250 pm in maximum diameter. (Demospongiae, Cladorhizidae) which will be de- The tissue contained 2, possibly 3, morphological types scribed in a forthcoming paper. Reference specimens of bacteria, distinctly different in size and ultrastruc- have bee.n deposited in the Museum National d'His- ture. Both common types were present in several dif- toire Naturelle in Paris (no. MNHN D JV 57). ferent extra- or intracellular locations throughout the Cytology. The specimens were fixed in 3% glu- sponge. The lateral appendages of the sponge, which taraldehyde in 0.4 M cacodylate buffer (pH 7.4) and were not examined by electron microscopy, appeared postfixed in 1% osmiun~tetroxide in the same buffer. under light microscopy to have the same organization They were dehydrated through an alcohol series and as the body. No gradient in the structure and distribu- embedded in Araldite. Thin sections were cut after tion of bacteria and bacteriocytes in the diverse zones local desilicification in 5 % hydrofluoric acid applied on of the sponge body was discernible. No difference was the free surface of the trimmed block (Borojevic & Levi observed between the samples from the 2 locations 1967). Semi-thin sections were stalned with toluidine (diatreme Atalante and Mount Manon). blue. Thln sections were contrasted with uranyl Extracellular symbionts were found at low density acetate and lead citrate, and observed under a Hitachi in the matrix of the sponge body among collagen fib- Hu 600 or Zeiss EM 912 transmission electron micro- rils (Fig. 2A, B). Their distribution was patchy, al- scope. though large clusters of symbionts were occasionally Tissue analyses. Key enzymes of methylotrophic and seen. A rough estimate of the volume of the various chemoautotrophic sulfur-oxidizing bacteria were tissue components made from TEM micrographs indi- tested as follows. RUBISCO (EC 4.1.1.39) activity was cated that the extracellular bacteria never exceed assayed by the method of Wishnick & Lane (1971) as 12% of the total tissue volume in the areas examined. modified by Felbeck (1981).Methanol dehydrogenase When extracellular, the symbionts were intact with no was assayed by the method of Anthony & Zathman slgns of degradation, and division stages were ob- (1965).ATP sulfurylase (EC 2.7 7.4)and ATP reductase served (Fig. 2B). (EC 1.8.99.2) were determined spectrophotometrically The symbionts were also abundant intracellularly in as described in Felbeck (1981). the sponge mesohyl (Fig. 2C. D). Symbionts were Tissue stable carbon and nitrogen isotope analyses observed in all cell types, including the sclerocytes were conducted on freeze-dried and acidified samples which secrete the siliceous spicules. The symbionts using standard methods with combustion techniques occurred either singly or loosely grouped in vacuoles by J. Boulegue and A. Mariotti (Universite P. et M. of diverse size (Fig. 2C, D), or crowded in large, round Curie, Paris, Laboratoire de Geochimie et Chimie vacuoles (Fig. 3). The different symbiont types were isotopique). The analyses were accomplished on a generally found in separate inclusions or vacuoles, Finningan Delta E mass spectrophotometer. Carbon is although they were occasionally seen together. Many reported relative to PDB (PeeDee Belernnite) and of the intracellular symbionts appeared to be in various nitrogen to atmospheric molecular nitrogen. stages in degradation, especially those crowded in the large vacuoles, suggesting lysosomal digestion by the host cell. Because of their d~stinctultrastructure, the RESULTS larger bacteria with stacked lamellae
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